REDIA, XCVII, 2014: 141-145 SHORT NOTE

SANJA RADONJIĆ (*) - SNJEŽANA HRNČIĆ (*) - CHRIS MALUMPHY (**)

FIRST RECORD OF ALEUROCANTHUS SPINIFERUS (QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGRO

(*) University of Montenegro, Biotechnical Faculty, Mihaila Lalića 1, 81000 Podgorica, Montenegro; e-mail: sanja_radonjic@t- com.me (**) The Food and Environment Research Agency, Sand Hutton, York, YO41 1LZ, United Kingdom

Radonjić S., Hrnčić S., Malumphy C. – First record of Aleurocanthus spiniferus (Quaintance) (Hemiptera Aleyrodidae) in Montenegro.

In October 2013, orange spiny whitefly Aleurocanthus spiniferus (Quaintance) (Hemiptera: Aleyrodidae) was detected for the first time in Montenegro. It was found in citrus orchards in Baošići (orange and mandarin), Herceg Novi (mandarin) and Kumbor (orange), in an area of Boka Kotor Bay on the Adriatic Sea (latitude 42° 26’ north). A. spiniferus is regulated in the European Union and therefore an immediate survey of the whole montenegrin coastal area, where citrus production occurs, was undertaken. The pest was additionally found in Djnovići, on a small number of mandarin and lemon trees. A. spiniferus is polyphagous and a major pest of citrus. It originated in south- east Asia and has spread widely in tropical and subtropical Asia, Africa and the Pacific Islands. In Europe it was first detected in Italy (2008) and subsequently in Croatia (2012). It presents a potential risk for citrus production in Montenegro, particularly for the important citrus producing areas of Bar and Ulcinj. These areas, geographically more southern than the area of first detection, are still free from the pest. Additionally, the whitefly presents a potential risk for other host plants grown in Montenegro where the climatic conditions are suitable for acclimatization of A. spiniferus.

KEY WORDS: Aleurocanthus spiniferus, Montenegro, first record, citrus pest.

INTRODUCTION between three to six generations per year (JANSEN, 2002). Each female lays 100+ eggs (WEEMS, 1974), and all Aleurocanthus spiniferus (Quaintance) (Hemiptera: developmental stages and occur on the undersurfaces of Aleyrodidae), commonly known as orange spiny whitefly, leaves. The adults fly actively when disturbed. originated in south-east Asia and has spread widely in A. spiniferus feeds on plant sap and excretes copious tropical and subtropical Asia, into Africa and the Pacific amounts of sugary, sticky honeydew, which coats the Islands (EPPO/CABI, 1997). It was recorded by Kuwana as leaves, branches and fruit surfaces. Black sooty mould the most destructive whitefly attacking citrus in tropical develops on the honeydew, reducing the area of Asia (KUWANA, 1928; WEEMS, 1974). This is a quarantine respiration and photosynthesis. A heavy infestation gives pest for the European Union. The genus Aleurocanthus the plants an almost completely black appearance. As a Quaintance & Baker (A. spiniferus and A. woglumi Ashby result, contaminated foliage may drop, young leaf growth are specifically listed) is regulated by EU Annex II/A1 is damaged, fruit set may be reduced, and already formed Council Directive 2000/29/EC (ANONYMOUS, 2000). A. fruits are unmarketable. Heavily infested plants suffer spiniferus is also listed by the European and Mediterranean from general weakening, dieback of branches and twigs, Plant Protection Organization (EPPO) as a species reco - deformed growth, and fruits are prematurely dropped mmended for regulation as a quarantine pest; it has recently (EPPO/CABI, 1997; CIOFFI et al., 2013). been transferred from the A1 (absent from the EPPO A. spiniferus was first detected in Europe in 2008 in region) to the A2 (locally present in the EPPO region) list the Apulia region of Southern Italy on oranges (ANONYMOUS, 2013). QUAINTANCE (1903) described the (PORCELLI, 2008). Since then it has been spreading in the species under the name Aleurodes spiniferus from specimens Apulia Region, gradually invaded the whole Lecce collected in Java (Indonesia) by Marlatt in 1901. District and expanding northward into Brindisi District A. spiniferus is a polyphagous pest that infests host plants (CIOFFI et al., 2013). A few years later, in May 2012, the assigned to more than 30 botanical families including pest was recorded in Croatia, on ornamental potted Ebenaceae, Lauraceae, Moraceae, Punicaceae, Rosaceae, orange seedlings (Citrus x aurantium L.) at one nursery Rutaceae and Vitaceae. CIOFFI et al. (2013) provided a garden in Split, a city on the coast of the Adriatic Sea, comprehensive list of its host plants. The main hosts of and action was taken to eradicate it (ŠIMALA and MASTEN economic importance are Citrus spp. MILEK, 2013). In October 2013, A. spiniferus was A. spiniferus has six developmental stages: the egg, four detected for the first time in citrus orchards in nymphal instars and the adult. In tropical conditions it has Montenegro and the purpose of this publication is to overlapping generations and all stages of A. spiniferus may provide details of this first incursion [an isolated be found throughout the year, although little breeding population of a pest recently detected in an area, not occurs during colder periods. The life cycle takes 2-4 known to be established, but expected to survive for the months depending on climatic conditions, and there can be immediate future (FAO, 2010)] in Montenegro.

– Received 10 June 2014 Accepted 30 September 2014 Published 10 December 2014 142 S. RADONJIĆ ET AL. REDIA, Vol. XCVII, 2014

MATERIALS AND METHODS in Baošići and Kumbor; in Kumbor it was found only on oranges while in Baošići it was found on both orange and In October 2013, the presence of a new whitefly mandarins (Fig. II). Several nymphs and eggs were also species in Montenegro was recorded in citrus orchards in found on one mandarin tree in a citrus orchard in Herceg Baošići, Kumbor and Herceg Novi, in the area of the Novi. After the initial finding of A. spiniferus an immediate Boka Kotor Bay on the Adriatic Sea (latitude 42° 26’ survey of the whole Montenegro coastal region, where north) (Fig. I). The whitefly colonies looked unusual as citrus production occurs, was undertaken in October, and repeated during November and December. The pest was the nymphs were black, surrounded by a fringe of white additionally found in Djenovići (near to where it was first wax, and the adults were metallic grey-blue with white detected), on a small number of mandarin and lemon trees. markings on their wings. During these inspections it was observed that the nymphs were more frequent on the undersurface of the older leaves, while the adults and eggs were more frequent on the undersurface of younger leaves.

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Fig. I. – Distribution of Aleurocanthus spiniferus in Montenegro (in red).

Samples of infested leaves were collected and taken to the Entomology Laboratory of the Biotechnical Faculty in Podgorica (Montenegro) for examination. Identity of the whitefly species was confirmed at The Food and Environment Research Agency (FERA) (United 2 Kingdom). A series of 10 puparia were slide mounted in Canada balsam according to the method by MALUMPHY (2004), examined using a Leitz Diaplan high power microscope (magnification x100-400) and identified on the basis of morphological characters using the descriptions and keys provided by MARTIN (1987), JANSEN (2002) and DUBEY and KO (2012). Voucher specimens are deposited at FERA. The Phytosanitary Directorate of Montenegro was officially informed about the first detection of A. spiniferus and additional surveys of the citrus producing areas in Montenegro were carried out in October, November and December, 2013.

RESULTS AND DISCUSSION 3

A. spiniferus adults, nymphs and eggs were recorded on the undersurface of leaves of several trees in citrus orchards Fig. II. – Colony of Aleurocanthus spiniferus on undersurface of orange leaf: nymphs (1, 2); adults (3). FIRST RECORD OF ALEUROCANTHUS SPINIFERUS (QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGRO 143

Colonies of A. spiniferus are highly conspicuous and elongate-oval with the lower surface convex and upper unlikely to be confused with any other whitefly species surface slightly concave, producing a kidney shape, 0.2 currently found in Europe. The field characteristics of mm long, and are usually laid in a characteristic spiral the species are shown in Fig. III, 1-6. Adult female A. pattern, attached to the undersurface of the leaves by a spiniferus are about 1.7 mm in length, and the males 1.35 short, slender pedicel extending from the lower surface mm long: at rest, their general appearance is metallic near the base of the egg. The chorion is covered with a grey-blue, being the colour of their wings which cover distinct lattice with little evidence of wax. The eggs are most of the body; a pale transverse mark across the yellowish when first laid, turning darker with maturity, middle of the wings is distinctive. The head and thorax becoming dark golden brown as the embryo develops. are dark red to brown, and the abdomen dark orange to Hatched eggs are a translucent golden brown. The first- red. The eyes are reddish-brown and the antennae and nymphal instar is elongate oval, with six well developed legs are white with pale-yellow markings. The eggs are legs, 0.30 x 0.15 mm, dusky in colour, with 2 pairs of

1 2

3 4

5 6

Fig III. – Aleurocanthus spiniferus: adult (1- resting pose, 2- female (left) and male (right)); elongate-oval to kidney-shaped eggs (3); eggs and young nymphs - 1st and 2nd instars (4); older nymphs 3rd and 4th instars and sooty mould (5); 4th instars - puparia (6) 144 S. RADONJIĆ ET AL. REDIA, Vol. XCVII, 2014 greatly enlarged dorsal setae (cephalic and first examination of the derm (external surface) of slide- abdominal). The second-nymphal instar is ovoid, slightly mounted puparia or empty pupal cases (as for all convex, with reduced, non-functional legs, 0.4 x 0.2 mm, Aleyrodidae) (JANSEN, 2002). Important diagnostic dark-brown to pale-black with yellow markings, with characters of the puparium of A. spiniferus include: easily distinguished, radiating spines; the third-nymphal puparium black; glandular spines present on all the dorsal instar is more ovate, 0.74-0.87 mm, generally black with a areas, apex of spines acute, most of them reaching well rounded, greenish spot on the anterior part of the beyond margin; female puparium with 30 pairs of dorsal abdomen, the spines are well developed and obvious; the spines, of which 11 pairs on submargin; all the submarginal fourth-nymphal instar, or puparium, is ovate, shiny- spines placed singly; abdominal submedian spines vary in black, with the females about 1.25 mm in length, and the length; vasiform orifice cordate with operculum almost males slightly smaller, about 1.0 mm in length. The dorsal filling the orifice; margin coarsely toothed with seven to surface bears many stout, glandular spines and there is a nine marginal teeth per 0.1 mm (Fig. IV, 1-2) (JANSEN, distinct white wax marginal secretion. Exuviae of earlier 2002; DUBEY and KO, 2012). A. spiniferus puparia are instars often remain stacked up on the median area of the morphologically similar to those of the related citrus puparium (EPPO/CABI, 1997). blackfly A. woglumi and may be separated using the key Identification to species requires microscopic presented by DUBEY and KO (2012).

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1 Fig. IV. – Aleurocanthus spiniferus: slide mounted female puparium (1); puparium margin showing the coarse marginal teeth (2)

The pathway of introduction of this quarantine species to plants or plant products and against their spread into Montenegro is unknown, as it has been recorded in within the Community + Annexes I-IX.- Official established citrus orchards (older than 10 years), with no Journal of the European Communities, L 169/29. recent import connection. It is assumed that the infestation ANONYMOUS, 2013 - EPPO A2 List of pests recommended is likely to have originated from plant material imported for regulation as quarantine pests (version 2013-09). from Italy or Croatia, where the pest has been found. Adults [online] URL: http://www.eppo.int/QUARANTINE/ of Aleurocanthus spp. are capable of limited down-wind listA2.htm flight, but this is not a major means of long-range dispersal. CIOFFI M., CORNARA D., CORRADO I., JANSEN M. G. M., The pest is most likely to be moved between countries on PORCELLI F., 2013 - The status of Aleurocanthus planting material of citrus or other host species, or possibly spiniferus from its unwanted introduction in Italy to on fruits. Species of Aleurocanthus have been intercepted on date.- Bulletin of Insectology, 66 (2): 273-281. the leaves of infested host plants moving in international DUBEY A.K., KO C.C., 2012 - Sexual dimorphism among trade (EPPO/CABI, 1997). species of Aleurocanthus Quaintance & Baker (Hemiptera: Aleyrodidae) in Taiwan, with one new species and an identification key. - Zootaxa, 3177: 1-23. REFERENCES EPPO/CABI, 1997 - Aleurocanthus spiniferus. In: SMITH I.M., MCNAMARA D.G., SCOTT P.R., HARRIS K.M., ANONYMOUS, 2000 - Council Directive 2000/29/EC of 8 (Eds.), 1997 - Quarantine Pests for Europe, Second May 2000 on protective measures against the Edition, CAB International, Wallingford: 21-24. introduction into the Community of organisms harmful F.A.O., 2010 - Glossary of phytosanitary terms. FIRST RECORD OF ALEUROCANTHUS SPINIFERUS (QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGRO 145

International standards for phytosanitary measures 5: spiniferus (Homoptera: Aleyrodidae) in Apulia, 1–27. Southern Italy. - Bulletin OEPP/EPPO Bulletin, 38: JANSEN M., 2002 - Diagnostic protocols for regulated pests. 518-520. Aleurocanthus spiniferus. - Bulletin OEPP/EPPO QUAINTANCE A. L., 1903 - New oriental Aleurodidae. - Bulletin, 32: 255-259. Canadian Entomologist, 35: 61-64. KUWANA, I., 1928 - Aleyrodidae or white flies attacking WEEMS H. V., 1974 - Orange spiny whitefly, citrus plants in Japan. - Ministry of Agriculture and Aleurocanthus spiniferus (Quaintance) (Homoptera: Forestry, Japan. Scientific Bulletin, 1:41-78. Aleyrodidae). - The Florida Department of Agriculture MALUMPHY C., 2004 - Diagnostic protocols for regulated and Consumer Services’ Division of Plant Industry pests – PM7/35 Bemisia tabaci. - Bulletin Entomology Circular, 151: 1-2. OEPP/EPPO Bulletin, 34: 281-288. ŠIMALA M., MASTEN MILEK T., 2013 - First Record of the MARTIN J.H., 1987 - An identification guide to common Orange Spiny Whitefly, Aleurocanthus spiniferus whitefly pest species of the world (Homoptera, Quaintance, 1903 (Hemiptera: Aleyrodidae), in Croatia. Aleyrodidae). - Tropical Pest Management, 33: 298– - Zbornik predavanj in referatov 11. Slovenskega 322. posvetovanja o varstvu rastlin z mednarodno udeležbo, PORCELLI F., 2008 - First record of Aleurocanthus 354-358.